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Amygdalofugal Modulation of Visceral Nociceptive Transmission in the Rat Caudal Ventrolateral Medulla under Normal Conditions and Intestinal Inflammation

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Abstract

The amygdala is one of the key limbic structures of the brain that provide central regulation of the autonomic nervous system. The central nucleus of the amygdala (CeA) is thought to play a leading role in the emotional and affective state-dependent assessment and modulation of viscerosensory information entering the brain, including nociceptive signals from the gastrointestinal tract. The recent data on neuroplastic changes in the CeA under colonic inflammation indicate that peripheral pathology can influence the amygdaloid control of visceral pain signaling. However, the specific mechanisms underlying such a control, as well as their alterations in organic diseases, remain poorly understood, hindering the development of effective abdominal pain treatments. The goal of the present neurophysiological experiments on anesthetized rats was to determine the neuronal mechanisms ensuring amygdalofugal modulation of the medullary visceral nociceptive transmission and to evaluate the features of their implementation during intestinal inflammation. For this purpose, the effects of electrical stimulation of the CeA on nociceptive colorectal distension (CRD)-evoked spike activity of neurons in the caudal ventrolateral medulla (CVLM) were studied in healthy animals and rats with experimental colitis. It was found that the CeA exerts a suppressive effect on the CVLM neural processing of nociceptive signals from the colon, as manifested in a decrease in excitatory and a weakening of inhibitory responses of medullary neurons to CRD. Since the observed effect may contribute to the attenuation of the ascending flow of nociceptive information and pain-triggered reflectory reactions implemented at the medullary level, it can be considered as antinociceptive. It was established that colitis is accompanied by a decrease in the inhibitory influence of the CeA on CRD-excited CVLM neurons while retaining the amygdalofugal suppression of inhibitory nociceptive neuronal responses. The revealed changes can lead to an enhancement of the supraspinal transmission of pain signals from the colon, i.e. underlie the central pathogenetic mechanisms of intestinal hyperalgesia and chronic abdominal pain.

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This work was carried out within the Program of Fundamental Research in State Academies of Sciences for 2013–2020.

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  1. Pavlov Institute of Physiology, Russian Academy of Sciences, St. Petersburg, Russia

    O. A. Lyubashina, I. B. Sivachenko & I. I. Busygina

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  1. O. A. Lyubashina
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Conceptualization and experimental planning (O.A.L.); data collection (I.B.S. and I.I.B.); data processing (O.A.L. and I.B.S.); writing and editing a manuscript (O.A.L., I.B.S., I.I.B.).

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Translated by A. Polyanovsky

Russian Text © The Author(s), 2021, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2021, Vol. 107, No. 10, pp. 1219–1234https://doi.org/10.31857/S086981392110006X.

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Lyubashina, O.A., Sivachenko, I.B. & Busygina, I.I. Amygdalofugal Modulation of Visceral Nociceptive Transmission in the Rat Caudal Ventrolateral Medulla under Normal Conditions and Intestinal Inflammation. J Evol Biochem Phys 57, 1150–1162 (2021). https://doi.org/10.1134/S0022093021050161

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